His first play, The Rennings Children, was chosen for the Stephen Sondheim-founded Young Playwrights, Inc. Young Playwright's Festival in 1982 while he was still an undergraduate. Lonergan matriculated to Wesleyan University where he trained as a playwright and director;[3] he would go on to graduate at the NYU Playwriting Program.

Lonergan directed his own screenplay for You Can Count On Me (2000); the film, which was executive produced by Martin Scorsese, went on to receive and be nominated for numerous writing awards.[6] He contributed to the screenplay for Gangs of New York (2002). In 2005, filming took place for his second film as writer/director, Margaret, starring Anna Paquin, Matt Damon, Matthew Broderick, and J. Smith-Cameron. The film spent over five years in post-production, with Lonergan, the producers and various editors unable to agree on its final cut, resulting in multiple legal disputes. It was finally released in 2011.[1]Margaret ranked 31st in a 2016 BBC poll of the 21st century's greatest films.[7]

Lonergan wrote and directed Manchester by the Sea, which was released in 2016 to critical acclaim.[8] He also had a small part in the film, as a pedestrian. David Fear of Rolling Stone said the film proves that Lonergan is "practically peerless in portraying loss as a living, breathing thing without resorting to the vocabulary of griefporn."[9]